Abstract
Background‘Candidatus Streptomyces philanthi’ is a monophyletic clade of formerly uncultured bacterial symbionts in solitary digger wasps of the genera Philanthus, Philanthinus and Trachypus (Hymenoptera, Crabronidae). These bacteria grow in female-specific antennal reservoirs and – after transmission to the cocoon – produce antibiotics protecting the host larvae from fungal infection. However, the symbionts’ refractoriness to cultivation has thus far hampered detailed in vitro studies on their physiology and on the evolutionary changes in metabolic versatility in response to the host environment.ResultsHere we isolated in axenic culture 22 ‘Streptomyces philanthi’ biovars from different host species. Sequencing of gyrB revealed no heterogeneity among isolates within host individuals, suggesting low levels of (micro)diversity or even clonality of the symbionts in individual beewolf antennae. Surprisingly, however, isolates from different host species differed strongly in their physiology. All biovars from the Eurasian/African Philanthus and the South American Trachypus host species had high nutritional demands and were susceptible to most antibiotics tested, suggesting a tight association with the hosts. By contrast, biovars isolated from the genus Philanthinus and the monophyletic North American Philanthus clade were metabolically versatile and showed broad antibiotic resistance. Concordantly, recent horizontal symbiont transfer events – reflected in different symbiont strains infecting the same host species – have been described only among North American Philanthus species, altogether indicative of facultative symbionts potentially capable of a free-living lifestyle. Phylogenetic analyses reveal a strong correlation between symbiont metabolic versatility and host phylogeny, suggesting that the host environment differentially affects the symbionts’ evolutionary fate. Although opportunistic bacteria were occasionally isolated from the antennae of different host species, only filamentous Actinobacteria (genera Streptomyces, Amycolatopsis and Nocardia) could replace ‘S. philanthi’ in the antennal gland reservoirs.ConclusionOur results indicate that closely related bacteria from a monophyletic clade of symbionts can experience very different evolutionary trajectories in response to the symbiotic lifestyle, which is reflected in different degrees of metabolic versatility and host-dependency. We propose that the host-provided environment could be an important factor in shaping the degenerative metabolic evolution in the symbionts and deciding whether they evolve into obligate symbionts or remain facultative and capable of a host-independent lifestyle.
Highlights
Mutualistic associations between invertebrate hosts and bacteria are widespread in nature [1] and have important implications for host ecology and evolution [2]
In antennal samples prepared for inoculation, ‘Ca. Streptomyces philanthi’ looked like individual or relatively short-chained unbranched cells; long mycelium, typical for free-living members this bacterial genus, was very rare
Fluorescence in situ hybridization (FISH) analysis demonstrated that the majority of these bacterial cells were physiologically active (Figure 1B)
Summary
Mutualistic associations between invertebrate hosts and bacteria are widespread in nature [1] and have important implications for host ecology and evolution [2]. More and more defensive alliances for the host’s protection against parasitoids, predators, and/or pathogens are being discovered [9,10], and filamentous Actinobacteria are especially prevalent as protective symbionts, due to their ability to produce a range of bioactive secondary metabolites [11,12]. Antibiotic-producing Actinobacteria have been implicated in pathogen defense of fungus gardens or galleries in leaf-cutter ants [13,14,15] and bark beetles [16], respectively, as well as in the protection of the developing offspring in solitary beewolf wasps [17]. Actinobacteria have been isolated from mud-dauber wasps [18], termites [19], the nests of Allomerus ants [20], and several other insect taxa, but their possible involvement in the protection of the hosts remains to be investigated
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